Reproduction is an essential human right that transcends race, gender, sexual orientation, or country of origin. Infertility is the impairment of reproductive capacity; it is a serious disease that affects 8-12% of couples of reproductive age and harms physical and mental well-being. Infertility is time-sensitive, and prognosis worsens with age. While there is no cure for most causes, the disease is most often treatable, and the majority of patients who seek treatment can ultimately become parents.

Defining the problem

The COVID-19 pandemic presents a unique global challenge on a scale not previously seen. The infectivity and mortality rates are higher than previous pandemics and the disease is present in almost every country. The propagation and containment have varied widely by location and, at present, the timeline to complete resolution is unknown. In the earliest stages of the pandemic, the American Society for Reproductive Medicine (ASRM) and the European Society of Human Reproduction and Embryology (ESHRE), independently recommended discontinuation of reproductive care except for the most urgent cases. More recently, with successful mitigation strategies in some areas and emergence of additional data, the societies have sanctioned gradual and judicious resumption of delivery of full reproductive care. In this document, ASRM, ESHRE and the International Federation of Fertility Societies (IFFS) have come together to jointly affirm the importance for continued reproductive care during the COVID-19 pandemic.

Reproductive medicine is essential

Reproductive care is essential for the well-being of society and for sustaining birth rates at a time that many nations are experiencing declines. During the pandemic, reproductive medicine professionals should continue to:

Advocate for the well-being of patients.

Monitor local conditions, including prevalence of disease, status of government or state regulations, and availability of resources.

Prioritize care and judiciously allocate use of limited resources using medical criteria.

Counsel patients about all options, including deferring evaluation and treatment.

Adhere to active risk mitigation strategies to reduce the risk of viral transmission.

Develop clear and codified plans to ensure the ability to provide care while maximizing the safety of their patients and staff.

Remain informed and stay current regarding new medical findings.

Develop or refine robust emergency plans.

Be prepared to interrupt medical treatment if conditions warrant discontinuation.

Research needed

In addition to helping patients, reproductive medicine practices are uniquely positioned to gather data and help to further COVID-19 research.

Reproductive medicine professionals and practices are essential front-line resources for screening, monitoring, and assessing the prevalence and impact of the disease on patients and their progeny through Point-of-Care data collection.

ESHRE, ASRM and IFFS are committed to continuous monitoring of the effects of COVID-19 on gametes and reproductive tissues, collecting data on pregnant patients infected during the pandemic, and assessing the outcomes of mothers and neonates.

Examples of these research and registry efforts follow:
a. In the U.S.A., the ASPIRE (Assessing the Safety of Pregnancy In the Coronavirus Pandemic) Study is a nationwide prospective cohort study of pregnant women and their offspring during the COVID-19 pandemic. All patients under the care of a reproductive medicine specialist who conceived spontaneously or with assisted reproductive technology (ART) between March 1st and December 31st are encouraged to participate.
b. ESHRE is gathering global case-by-case reporting on the outcome of medically assisted reproduction (MAR) conceived pregnancies in women with a confirmed infection (https://nl.surveymonkey.com/r/COVID19ART).
c. The affiliate society of ASRM, the Society for Assisted Reproductive Technologies (SART) is including mandatory COVID-19-related questions in their Clinic Outcome Reporting System (CORS) registry of assisted reproductive technologies (ART), which accounts for over 95% of all ART cycles in the U.S.A.
d. ESHRE is gathering data and mapping MAR/ART activity during the pandemic, country by country whether and /or when they stopped offering treatment and when they have resumed care.
e. IFFS is conducting COVID-19-related periodic surveys to assess global trends in access to MAR/ART services.

Final thoughts

Reproductive care is essential and reproductive medicine professionals are in a unique position to promote health and wellbeing. In addition, ASRM, ESHRE and IFFS are collaborating to advocate for patients and to gather data and resources to enhance the understanding of COVID-19 as it pertains to reproduction, pregnancy, and the impact on the fetus and neonate. The lessons learned from these experiences will be useful as humanity deals with future pandemics.

Karl-Gösta Nygren, known to his colleagues in Sweden as 'KG', died peacefully on 12 May following a brief period in hospital with coronavirus infection. ESHRE is now honoured to record the enormous contribution Karl made to the Society over many years and to express deep sadness at his death.

Members and colleagues will remember Karl for his tireless work on monitoring ART activity and safety through registry data. There had been some international interest in IVF surveillance when in 1998 Karl and his Danish colleague Anders Nyboe Andersen made a formal proposal to the executive committee that ESHRE should take responsibility for collecting IVF data in Europe. It would be a huge logistical undertaking, dependent on comprehensive data collection for its reliability, and an exercise which would take shape as the European IVF Monitoring (EIM) consortium for ESHRE - with Karl its first chairman. Since its first report on activity in 1997, the consortium has monitored cycles increasing by about 10% per year, and a cumulative total of around 10 million, with some 2 million children born. And collecting data on a single procedure is no longer a simple matter of recording a cycle, as was first proposed, but must now acknowledge oocyte and/or embryo cryopreservation, transfer in a fresh or future cycle, and outcome, which may well be several years after the initial egg collection.

For ESHRE the inspiration of Karl and Anders Nyboe Andersen has now become one of its most powerful and influential activities, with all now agreed that monitoring such systems as ART are mandatory for clinical science to progress. EIM reports continue to be some of the most highly cited papers in the ESHRE journals.

Karl-Gösta Nygren was Associate Professor of Obstetrics and Gynaecology at the Sophiahemmet clinic in Stockholm, which he established in 1984 as Sweden's first private IVF centre and where he would remain throughout his career. He served on many committees, notably ESHRE's advisory committee of national representatives and later as coordinator of the SIG Safety and Quality in ART. He was elected chairman of the International Committee Monitoring ART (ICMART) at its first board meeting in 2003 to coordinate its world surveillance programme, and was president of the Swedish Society for Obstetricians and Gynaecologists between 1992 and 1994.

In 2007, in a report highlighting a 5% twin rate in IVF in Sweden, he predicted that single embryo transfer 'will become the norm' in the treatment of infertility, and throughout his career he continued to support SET as a necessary requirement of IVF safety. It was Karl, whose personal rallying cry was 'Safety first', who came up with the 'one child at a time' slogan, which many would take up in campaigns to reduce their multiple pregnancy rate. And applying the data generated by Sweden's registry systems, he was the author of many cross-linkage studies assessing the long-term safety of IVF. Multiplicity was invariably associated with adverse outcomes in these studies.

Karl was a member of ESHRE's executive committee from 1997 to 2001 and was an ever cheerful fixture at annual meetings and Campus events, where he continued to enjoy the company of members and colleagues. He was made an honorary member of ESHRE in 2005. His contribution to the Society in the foundation and running of the EIM consortium has been monumental and ESHRE is honoured to express its gratitude for his work and its condolences to his wife Margareta and family.

Former ESHRE chair Kersti Lundin remembers Karl as 'a very important person for ART in Sweden and in the world'. 'I first met him when I was a young embryologist in Gothenburg,' she recalls, 'and was fascinated by his determination and stamina in fighting for patient rights to best treatment and for the health of the children. He was a very kind and generous man, with a great sense of humour, but he would rarely give way in any discussion on matters close to his heart. He was a good friend and part of my upbringing in ART, and I, like many others, will remember him with great fondness.'

As the COVID-19 pandemic is stabilising, the return to normal daily life will also see the need to restart the provison of ART treatments. Infertility is a disease and once the risk of SARS-CoV-2/COVID-19 infection is decreasing, all ART treatments can be restarted for any clinical indication, in line with local regulations.

However, vigilance and measured steps must be taken for safe practice and to minimise the risks related to SARS-CoV-2/COVID-19-positive patients or staff during treatment.
The ESHRE COVID-19 working group has prepared the “ESHRE Guidance on recommencing ART treatments”, a set of recommendations for centres planning to restart ART treatments.

In view of the continuing prevalence of infection from the coronavirus SARS-CoV-2 (i.e. the virus causing COVID-19) and widespread initiatives to limit its spread, ESHRE reaffirms its recommendation to follow local and national government advice, particularly national daily updates.

The available evidence

To date, there is no clear evidence of any negative effect of SARS-CoV-2 infection on pregnancy, as indicated by the latest updates from the Centers for Disease Control and Prevention (CDC) in the USA and others in Europe.[1, 2] Even so, we should be mindful that viral infections can be more problematic for pregnant women and acknowledge that some of the medications used in virus-infected patients may not be recommended during pregnancy.

Recent updates on pregnancy outcomes in infected mothers report healthy infants born free of the disease.[3] However, there are small case series reporting adverse outcomes, such as premature rupture of membranes and preterm delivery.[4] Neonatal SARS-CoV-2 infection (five cases) [5-7] and the presence of IgM (and IgG) antibodies against the virus in newborns (three cases) [8, 9] have also been reported. It is unclear whether these data are indicative of vertical transmission of SARS-CoV-2.

An up-to-date overview of data extracted from all published reports on pregnancy and neonatal outcomes in women with confirmed COVID-19 is available from the Cochrane Gynaecology and Fertility Group (https://cgf.cochrane.org/news/covid-19-coronavirus-disease-fertility-and-pregnancy). In general, the data on pregnancy outcomes, although reassuring, only report small numbers and must be interpreted with caution. Furthermore, as reports mainly refer to infection in the third trimester, there is no information on the possible effect of SARS-CoV-2 infection on pregnancies in their initial stages.[10]

ESHRE’s guidance

In view of the above considerations and outcomes reported in cases of other coronavirus infections (such as SARS and MERS) [11, 12], ESHRE continues to recommend a precautionary approach to assisted reproduction, which is consistent with the position of other scientific societies in reproductive medicine. During the pandemic, all medical professionals have a duty to avoid contributing additional stress to a healthcare system that in many locations is already overloaded.

ESHRE advises that assisted reproduction treatments should not be started at present for the following reasons:

- To avoid complications from assisted reproduction treatment and pregnancy
- To avoid potential SARS-CoV-2 related complications during pregnancy
- To mitigate the unknown risk of vertical transmission in SARS-CoV-2 positive patients
- To support the necessary reallocation of healthcare resources
- To observe the current recommendations of social distancing.

In cases of urgent fertility preservation in oncology patients, the cryopreservation of gametes, embryos or tissue should still be considered.

For those patients having started assisted reproduction treatment at the present time, elective oocyte or embryo freezing for later embryo transfer (freeze-all) is recommended.

Any risk of viral contamination to gametes and embryos in the IVF laboratory, either from infected patients or professionals, is likely to be minimal (if at all) because the repeated washing steps required for the culture and freezing protocols will result in a high dilution of any possible contaminants.Even with no specific data available, it is assumed that sperm, oocytes and embryos are unlikely to be infected. Furthermore, the zona pellucida represents a high level of protection for oocytes and embryos. Regardless of the biological details, it is prudent to defer all elective fertility-promoting medical procedures, primarily to maintain social distancing and protect any and all medical resources.

Since many uncertainties remain about the effects of SARS-CoV-2 infection on ART and pregnancy, and despite different approaches among treatment centres and countries, ESHRE currently considers any risk too high when similar treatments can be performed at a later date.

Healthcare professionals and clinics should remain available to provide supportive care , psychological support and clinical advice to their patients, preferably via online consultation.
As always, good clinical and laboratory practice is strongly recommended by ESHRE to guarantee safety for processed tissues and cells, professionals and patients. [13, 14]

ESHRE will continue to monitor the scientific literature and this statement will be regularly updated.

The ESHRE COVID-19 working group is presently preparing recommendations for clinics planning to restart ART services. These will consider patient selection, general and specific organisation of services and good laboratory and clinical practice, with an emphasis on both patient and professional safety and responsibilities.

In view of the rapidly growing number of reports and the impact of the COVID-19 coronavirus on public health, ESHRE has formed a specialist working group to keep track of bibliography and published scientific reports relevant to reproductive medicine, pregnancy and newborns.

It is hoped that the data assembled will consolidate and lead ESHRE's response to the impact of COVID-19 on pregnancy and reproductive health.

'There are scientific reports on the coronavirus published every day,' said Coordinator Anna Veiga, 'and our group will screen them for developments in reproductive health and pregnancy. Our first aim will be to ensure ESHRE guidance is up-to-date and accurate, but we also hope this will become an ESHRE resource centre for everyone working in reproduction.'

The working group's aims are to:

Keep track of emerging data

Ensure a timely update of ESHRE guidance

Provide the substance for quick and accurate response to emerging questions from professionals, patients and the press

Be available to answer press questions on new scientific developments

A daily report will be prepared by ESHRE Central Office from the working group's monitoring activities.

23 March 2020 - It is with great regret that ESHRE today announces cancellation of its 2020 Annual Meeting planned for Copenhagen on 5-8 July. Many of you, ESHRE members and colleagues, will not be surprised: indeed, with long-term protection measures against the coronavirus now in place, restrictions on public gatherings, and flight schedules unlikely to be resumed soon, cancellation had rapidly become inevitable.

'It's an extremely disappointing decision to take,' said ESHRE Chair Cristina Magli, 'but we are all aware of the devastating effects of COVID-19. Prevention and protection must be our priorities. We did consider postponement, but this is an annual event attended by more than 10,000 people from all over the world. Postponement and re-arrangement were impossible. ESHRE remains a strong and well supported Society and it is our hope that the energy and scientific advances made by our supporters this year will continue to drive our next meeting in Paris in 2021.'

ESHRE is now exploring the possibility of developing a virtual platform for the availability of intended 2020 presentations online. This would hopefully be a simple process, and all speakers will now be contacted about their willingness to participate - but this project is still in the planning stages. Thus, the abstracts review process and programme planning will continue, and all those submitting an abstract will be informed in due course if it was selected for presentation.

All those who have already registered for Copenhagen 2020 will also be contacted about refunding their payments.

Cancellation of this year's meeting has implications for many related activities, for which ESHRE cannot yet provide detailed information. Precongress courses and certification exams scheduled for Copenhagen must now be cancelled and rearranged; once clarified, details, including refund of fees, will be distributed. Also cancelled or postponed are all Campus meetings scheduled for May.

Despite the loss of this year's annual meeting, please be assured that ESHRE, its online activities and website will remain as active as ever during the next difficult weeks. We are determined that ESHRE’s opportunities for education and leadership are not suppressed by these most unfortunate circumstances. And we hope we can rely on your continued support and understanding at this unprecedented time.

In view of the increasing incidence of infection from the coronavirus Covid-19 and widespread initiatives to limit its spread, ESHRE reaffirms its recommendation that Society members follow local and national government advice, particularly national daily advice updates, with compliance encouraged where feasible.

Pregnancy and conception

There is no strong evidence of any negative effects of Covid-19 infection on pregnancies, especially those at early stages, as indicated by the latest updates from the Centers for Disease Control and Prevention (CDC) in the USA and others in Europe.(1,2)

There are a few reported cases of women positive for Covid-19 who delivered healthy infants free of the disease.(3) There have been reports of adverse neonatal outcomes (premature rupture of membranes, preterm delivery) in infants born to mothers positive for Covid-19 during their pregnancy, but the reports were based on limited data.(4,5) Similarly, one case report has been published of an infected infant, but again there was no strong evidence that this was the result of vertical transmission.(6)

These data, although encouraging, only report small numbers and must be interpreted with caution. They refer to pregnancies in their final stages, but we have no information on the possible effect of Covid-19 infection on pregnancies in their initial stages.(7)

However, in view of the above considerations and the maternal and neonatal outcomes reported in cases of other coronavirus infections (such as SARS), ESHRE continues to recommend a precautionary approach.(8) It is also important to note that some of medical treatment given to severely infected patients may indicate the use of drugs which are contraindicated in pregnant women.

As a precautionary measure - and in line with the position of other scientific societies in reproductive medicine - we advise that all fertility patients considering or planning treatment, even if they do not meet the diagnostic criteria for Covid-19 infection, should avoid becoming pregnant at this time. For those patients already having treatment, we suggest considering deferred pregnancy with oocyte or embryo freezing for later embryo transfer.

ESHRE further advises that patients who are pregnant or those (men and women) planning or undergoing fertility treatment should avoid travel to known areas of infection and contact with potentially infected individuals.

ESHRE will continue to monitor the scientific literature, especially in relation to ART and pregnancy. And reaffirms the view that all medical professionals have a duty to avoid additional stress to a healthcare system that in many locations is already overloaded.

It was with great sadness that ESHRE learned of the death of Lynn Fraser, chair of ESHRE from 1999 to 2001 and the first female to lead the Society. Lynn, a biologist with a research interest in sperm function, had an extensive involvement with ESHRE, moving from the Advisory Committee in 1990 to become two years later co-ordinator of the newly founded Special Interest Group Andrology. She joined the Executive Committee the following year and in 1999 became the Society's first female chair, taking charge of ESHRE during the two most difficult years of its history.

Lynn Fraser grew up and was educated in the USA. She took her first degree in zoology at the University of Colorado and her doctorate at Yale, where she was awarded a Ford Foundation postdoctoral fellowship. In 1972 she moved to London to take up a scientific post for the Medical Research Council, where she remained for five years. In 1977 she became a lecturer at King's College, London, and in 1993 Professor of Reproductive Biology. From 1991 Lynn was also an inspector for the UK's Human Fertilisation and Embryology Authority.

The years of Lynn's chairmanship of ESHRE were noted for their divided views on the publication model of the ESHRE journals. Robert Edwards, who had edited Human Reproduction from its foundation in 1985 and in the meantime had introduced Molecular Human Reproduction and Update, favoured self-publication, while the Executive Committee preferred to rely on the proven support of a commercial publisher. It was Lynn's task to steer ESHRE's way through these divided opinions and to ensure through unanimity the continuing success of the journals.

After her academic retirement in 2003, Lynn retained her great interest in ESHRE and its progress, and was always to be seen at every annual meeting, enjoying the social gatherings and the company of her fellow past chairs. She had not been well for the past few months and ESHRE is honoured to express its gratitude for her work and its condolences to her husband Bill and family.

Hans Evers, who succeeded Lynn as ESHRE chairman in 2001, recalls how he learned 'to appreciate Lynn's wise governance and her gifts as a considerate moderator', adding: 'She always was at her best when strong opinions were in conflict, and when irreconcilable opponents needed an honourable escape. Otherwise, we will always remember Lynn and Bill (the first man in our annual meeting's spouses programme) for their congeniality, their great social skills and their delightful and entertaining dinner talks.'

It is with great regret that ESHRE is postponing its Campus meetings scheduled for March and April. ESHRE has been closely monitoring the spread and prevention of the coronavirus Covid-19 and has taken this decision in the light of present circumstances.

The following Campus meetings, originally planned for March and April 2020, have now been postponed:

27-28 March 2020, Top quality in ultrasound - Bucharest, Romania, has been postponed to 25-26 September 2020

2-4 April 2020, Reproduction, hormones and the brain - Amsterdam, the Netherlands, has been postponed to 6-8 May 2021

14-15 May 2020, Counselling in third party reproduction – Amsterdam, The Netherlands, will be postponed to 28-29 January 2021

21-23 May 2020, ‘Haute Cuisine’ of the IVF laboratory – Barcelona, Spain, will be postponed to 20-22 May 2021

'
We have been monitoring the situation closely,' said ESHRE Chair Cristina Magli, ' but in the end, with increasing infection rates, travel restrictions and more international prevention measures in place, we considered postponement our best option given that avoiding personal contact is the only way to stop spread of the virus. We hope all ESHRE members and colleagues understand and support our decision.'

ESHRE will try to re-arrange these meetings at later dates with the SIG organisers and will inform all registrants individually about new arrangements. Meanwhile, answers to some of your questions may be found here.